Abstract
Determining the distribution and abundance of populations is the first step toward assessing biodiversity conservation status. This step is based on field observations that are largely influenced by the sampling method employed. Autonomous Recording Units (ARUs) are tools developed to improve species monitoring that employ acoustic communication. Although largely employed, the efforts required to achieve good diversity estimates with this technique are still unknown. We investigate the use of ARUs in estimating species richness of anuran assemblages in a tropical region, aiming to determine the sampling sufficiency of species richness at local and regional levels, analyze whether the asymptote point is related to forest cover, and investigate the influence of subsampling type over time on species richness estimates. We monitored amphibians in 14 streams embedded in landscapes representing a gradient from 20 to 70% native forest coverage. We detected a total of 14 species, with the regional sampling sufficiency of total species richness reached in 3448 min and influenced mainly by the terrestrial species’ presence. Forest coverage had no influence on the minimum audio processing time required to achieve local asymptote. The subsampling schemes (temporally stratified and randomly assigned) had similar efficiency when using 5 min/h or more sample efforts. Our findings indicate that passive acoustic monitoring can adequately represent local anuran richness, focusing especially on the arboreal guild. Sampling effort can be optimized, with a 5 min/h duty cycle being sufficient to recover detection of most species, saving up to 75% of the effort devoted to auditing the acoustic dataset.
Similar content being viewed by others
Data availability
The data that support the findings of this study are available from the corresponding author, PRA, upon reasonable request.
References
Acevedo MA, Vilanueva-Rivera LJ (2006) Using automated digital recording systems as effective tools for the monitoring of birds and amphibians. Wildl Soc Bull 34:211–214. https://doi.org/10.2193/0091-7648(2006)34[211:uadrsa]2.0.co;2
Alvarez-Berríos N, Campos-Cerqueira M, Hernández-Serna A, Delgado CJA, Aide R-D (2016) Impacts of small-scale gold mining on birds and anurans near the Tambopata Natural Reserve, Peru, assessed using passive acoustic monitoring. Trop Conserv Sci 9:832–851. https://doi.org/10.1177/194008291600900216
Araújo CB, Jardim M, Saturnino NSF, Rosa GM, Lima MR, dos Anjos L (2020) The optimal listening period for an effective assessment of bird richness and composition: a case study of Neotropical Forest. J Ornithol. https://doi.org/10.1007/s10336-020-01812-6
Arntzen JW, Abrahams C, Meilink WRM, Iosif R, Zuiderwijk A (2017) Amphibian decline, pond loss and reduced population connectivity under agricultural intensification over a 38-year period. Biodivers Conserv 26(6):1411–1430. https://doi.org/10.1007/s10531-017-1307-y
Almeida-Gomes M, Rocha CFD (2015) Habitat loss reduces the diversity of frog reproductive modes in an atlantic forest fragmented landscape. Biotropica 4(1):113–118. https://doi.org/10.1111/btp.12168
Bardeli R, Wolff D, Kurth F, Koch M, Tauchert KH, Frommolt KH (2010) Detecting bird sounds in a complex acoustic environment and application to bioacoustic monitoring. Pattern Recognit Lett 31:1524–1534. https://doi.org/10.1016/j.patrec.2009.09.014
Baêta D, Giasson LOM, Pombal JP, Haddad CFB (2016) Review of the rare genus Phrynomedusa Miranda-Ribeiro, 1923 (Anura: Phyllomedusidae) with description of a new species. Herpetol Monogr 30(1):49–78. https://doi.org/10.1655/HERPMONOGRAPHS-D-15-00009.1
Becker CG, Zamudio KR (2011) Tropical amphibian populations experience higher disease risk in natural habitats. PNAS 108(24):9893–9898. https://doi.org/10.1073/pnas.1014497108
Becker CG, Fonseca CR, Haddad CFB, Batista RF, Prado PI (2007) Habitat split and the global decline of amphibians. Science 318:1775–1777. https://doi.org/10.1126/science.1149374
Benício RA, Silva FR (2017) Amphibians of Vassununga State Park, one of the last remnants of semideciduous Atlantic Forest and Cerrado in northeastern São Paulo state, Brazil. Biota Neotrop 17:1–7. https://doi.org/10.1590/1676-0611-bn-2016-0197
Bertoluci J, Rodrigues MT (2002) Seasonal patterns of breeding activity of Atlantic Rainforest anurans at Boracéia, Southeastern Brazil. Amphib Reptil 23:161–167. https://doi.org/10.1163/156853802760061804
Bioacoustics Research Program (2014) Raven Pro: Interactive Sound Analysis Software (Version 1.5) [Computer software]. The Cornell Lab of Ornithology, Ithaca http://www.birds.cornell.edu/raven.
Blumstein DT, Mennill DJ, Clemins P, Girod L, Yao K, Patricelli G, Deppe JL, Krakauer AH, Clark C, Cortopassi KA, Hanser SF, Mccowan B, Ali AM, Kirschel ANG (2011) Acoustic monitoring in terrestrial environments using microphone arrays: Applications, technological considerations and prospectus. J Appl Ecol 48:758–767. https://doi.org/10.1111/j.1365-2664.2011.01993.x
Brauer CL, Donovan TM, Mickey RM, Katz J, Mitchell BR (2016) A comparison of acoustic monitoring methods for common anurans of the northeastern United States. Wildl Soc Bull 40:140–149. https://doi.org/10.1002/wsb.619
Browning E, Gibb R, Glover-Kapfer P, Jones KE (2017) Passive acoustic monitoring in ecology and conservation. Woking, UK
Buckley LB, Hurlbert AH, Jetz W (2012) Broad-scale ecological implications of ectothermy and endothermy in changing environments. Glob Ecol Biogeogr 21:873–885. https://doi.org/10.1111/j.1466-8238.2011.00737.x
Campos VA, Oda FH, Juen L, Barth A, Dartora A (2013) Composição e riqueza de espécies de anfíbios anuros em três diferentes habitat em um agrossistema no Cerrado do Brasil central. Biota Neotrop 13:124–132. https://doi.org/10.1590/S1676-06032013000100014
Carey M, Boland J, Weigelt P, Keppel G (2020) Towards an extended framework for the general dynamic theory of biogeography. J Biogeogr 47:2554–2566. https://doi.org/10.1111/jbi.13944
Chao A, Gotelli NJ, Hsieh TC, Sander EL, Ma KH, Colwell RK, Ellison AM (2014) Rarefaction and extrapolation with Hill numbers: A framework for sampling and estimation in species diversity studies. Ecol Monogr 84:45–67. https://doi.org/10.1890/13-0133.1
Costa WP, Almeida SC, Jim J (2013) Anurofauna em uma área na Depressão Periférica, no centro-oeste do estado de São Paulo Brasil. Biota Neotrop 13:15. https://doi.org/10.1590/S1676-06032013000200015
Cruz CAG, Pimenta B (2004) Phrynomedusa fimbriata. The IUCN Red List of Threatened Species 2004: e.T17078A6797217. https://dx.doi.org/https://doi.org/10.2305/IUCN.UK.2004.RLTS.T17078A6797217.en. Accessed 11 August 2022
Cushman SA (2006) Effects of habitat loss and fragmentation on amphibians: a review and prospectus. Biol Conserv 128(2):231–240. https://doi.org/10.1016/j.biocon.2005.09.031
Darras K, Batáry P, Furnas B, Celis-Murillo A, Van Wilgenburg SL, Mulyani YA, Tscharntke T (2018) Comparing the sampling performance of sound recorders versus point counts in bird surveys: a meta-analysis. J Appl Ecol 55:2575–2586. https://doi.org/10.1111/1365-2664.13229
Digby A, Towsey M, Bell BD, Teal PD (2013) A practical comparison of manual and autonomous methods for acoustic monitoring. Methods Ecol Evol 4:675–683. https://doi.org/10.1111/2041-210X.12060
Doan T (2003) Which methods are most effective for surveying rain forest herpetofauna? J Herpetol 37(1):72–81.https://doi.org/10.1670/0022-1511(2003)037[0072:WMAMEF]2.0.CO;2
Dorcas ME, Price JT, Walls SC, Barichivich WJ (2009) Auditory monitoring of anuran populations. In: Dodd CK (ed) Amphibian ecology and conservation. Oxford University Press, Oxford, pp 281–298
D’Anunciação PER, Silva MFV, Ferrante L, Assis DS, Casagrande T, Coelho AZG, Amâncio BCS, Pereira TR, Silva VX (2013) Forest fragments surrounded by sugar cane are more inhospitable to terrestrial amphibian abundance than fragments surrounded by pasture. Int J Ecol 15:1–8
Emmrich M, Vences M, Ernst R, Köhler J, Barej MF, Glaw F, Jansen M, Rödel MO (2020) A guild classification system proposed for anuran advertisement calls. Zoosystematics Evol 96:515–525. https://doi.org/10.3897/zse.96.38770
Eterovick P, Carnaval ACOQ, Borges-Nojosa DM, Silvano DL, Segalla MV, Sazima I (2005) Amphibian declines in Brazil: an overview. Biotropica 37(2):166–179. https://doi.org/10.1111/j.1744-7429.2005.00024.x
Ferreira RB, Beard KH, Crump ML (2016) Breeding guild determines frog distributions in response to edge effects and habitat conversion in the Brazil’s Atlantic forest. PLoS ONE 11(6):e0156781. https://doi.org/10.1371/journal.pone.0156781
Francomano D, Gottesman BL, Pijanowski BC (2020) Biogeographical and analytical implications of temporal variability in geographically diverse soundscapes. Ecol Indic 112:105845. https://doi.org/10.1016/j.ecolind.2019.105845
Gardner TA, Barlow J, Peres CA (2007) Paradox, presumption and pitfalls in conservation biology: the importance of habitat change for amphibians and reptiles. Biol Conserv 138(1–2):166–179. https://doi.org/10.1016/j.biocon.2007.04.017
Gibb R, Browning E, Glover-Kapfer P, Jones KE (2019) Emerging opportunities and challenges for passive acoustics in ecological assessment and monitoring. Methods Ecol Evol 10:169–185. https://doi.org/10.1111/2041-210X.13101
Gotelli NJ, Colwell RK (2001) Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol Lett 4:379–391. https://doi.org/10.1046/j.1461-0248.2001.00230.x
Guerra V, de Queiroz CN, Llusia D, Márquez R, Bastos RP (2020a) Nightly patterns of calling activity in anuran assemblages of the Cerrado, Brazil. Community Ecol 21:33–42. https://doi.org/10.1007/s42974-020-00013-8
Guerra V, Jardim L, Llusia D, Marquez R, Bastos RP (2020b) Knowledge status and trends in description of amphibian species in Brazil. Ecol Indic 118:106754. https://doi.org/10.1016/j.ecolind.2020.106754
Guerry AD, Hunter ML Jr (2018) Society for conservation biology amphibian distributions in a landscape of forests and agriculture: an examination of landscape composition and configuration. Conserv Biol 16:745–754. https://doi.org/10.1046/j.1523-1739.2002.00557.x
Hill JL, Curran PJ, Foody GM (1995) The effect of sampling on the species-area curve. Glob Ecol Biogeogr Lett 4:97–106. https://doi.org/10.2307/2997435
Hilton-Taylor C, Pollock CM, Chanson JS, Butchart SHM, Oldfield TEE, Katariya V (2009) State of the world’s species. Pages 15–41 in world - an analysis of the 2008 IUCN Red List of Threatened Species. International Union for Conservation of Nature, Gland
Houlahan JE, Findlay CS (2003) The effects of adjacent land use on wetland amphibian species richness and community composition. Can J Fish Aqua Sci 60:1078–1094. https://doi.org/10.1139/f03-095
Hsieh TC, Ma KH, Chao A (2016) iNEXT: iNterpolation and EXTrapolation for species diversity. R package version 2.0.12 URL: http://chao.stat.nthu.edu.tw/blog/software-download/.
Hutto RL, Stutzman RJ (2009) Humans versus autonomous recording units: a comparison of point-count results. J F Ornithol 80:387–398. https://doi.org/10.1111/j.1557-9263.2009.00245.x
IBGE (2010) Instituto Brasileiro de Geografia e Estatística. Censo Demográfico. Available online at. https://www.ibge.gov.br/. Accessed 13 October 2020
Kluber MR, Olson DH, Puettmann KJ (2008) Amphibian distributions in riparian and upslope areas and their habitat associations on managed forest landscapes in the Oregon Coast Range. For Ecol Manage 256:529–535. https://doi.org/10.1016/j.foreco.2008.04.043
Koblitz RV, Lima AP, Menin M, Rojas D, Condrati LH, Magnusson WE (2017) Effect of species-counting protocols and the spatial distribution of effort on rarefaction curves in relation to decision making in environmental-impact assessments. Austral Ecol 42:723–731. https://doi.org/10.1111/aec.12490
Köhler J, Jansen M, Rodríguez A, Kok PJR, Toledo LF, Emmrich M, Glaw F, Haddad CFB, Rödel MO, Vences M (2017) The use of bioacoustics in anuran taxonomy: theory, terminology, methods and recommendations for best practice. Zootaxa 4251:1–124. https://doi.org/10.11646/zootaxa.4251.1.1
Laiolo P (2010) The emerging significance of bioacoustics in animal species conservation. Biol Conserv 143:1635–1645. https://doi.org/10.1016/j.biocon.2010.03.025
MacArthur RH, Wilson EO (1967) The theory of island biogeography. Princeton University Press, Princeton
Mack AL, Alonso LE (2000) A biological assessment of the Wapoga River area of Northwestern Irian Jaya, Indonesia. Rapid Assessment Program Bulletin of Biological Assessment 14, Conservation International, Washington
Madalozzo B, Santos TG, Santos MB, Both C, Cechin S (2017) Biodiversity assessment: selecting sampling techniques to access anuran diversity in grassland ecosystems. Wildl Res 44(1):78–91. https://doi.org/10.1071/WR16086
Maffei F, Do Nascimento BTM, Moya GM, Donatelli RJ (2015) Anurans of the Agudos and Jaú municipalities, state of São Paulo Southeastern Brazil. Check List 11(3):1645. https://doi.org/10.15560/11.3.1645
Magurran AE (2003) Measuring biological diversity. Wiley, Oxford
Martello F, De Bello F, De Castro Morini MS, Silva RR, De Souza-Campana DR, Ribeiro MC, Carmona CP (2018) Homogenization and impoverishment of taxonomic and functional diversity of ants in Eucalyptus plantations. Sci Rep 8:1–11. https://doi.org/10.1038/s41598-018-20823-1
Melo GL, Sponchiado J, Cáceres NC, Fahrig L (2017) Testing the habitat amount hypothesis for South American small mammals. Biol Conserv 209:304–314. https://doi.org/10.1016/j.biocon.2017.02.031
Melo I, Llusia D, Bastos RP, Signorelli L (2021) Active or passive acoustic monitoring? Assessing methods to track anuran communities in tropical savanna wetlands. Ecol Indic 132:108305. https://doi.org/10.1016/j.ecolind.2021.108305
Montambault JR, Missa O (2002) A biodiversity assessment of the Eastern Kanuku Mountains, Lower Kwitaro River, Guyana. Rapid Assessment Program Bulletin of Biological Assessment 26. Conservation International, Washington
Morellato LPC, Haddad CFB (2000) Introduction: the Brazilian Atlantic Forest. Biotropica 32:786–792. https://doi.org/10.1111/j.1744-7429.2000.tb00618.x
Moura MR, Jetz W (2021) Shortfalls and opportunities in terrestrial vertebrate species discovery. Nat Ecol Evol 5(5):631–639. https://doi.org/10.1038/s41559-021-01411-5
Muylaert RL, Vancine MH, Bernard R, Oshima JEF, Sobral-Souza T, Tonetti VR, Niebuhr BB, Ribeiro MC (2018) A note on the territorial limits of the Atlantic forest. Oecologia Aust 22:302–311. https://doi.org/10.4257/oeco.2018.2203.09
Obrist MK, Pavan G, Sueur J, Riede K, Llusia D, Marquez R (2010) Bioacoustics approaches in biodiversity inventories. Abc Taxa 8:68
Parris KM, Norton WT, Cunningham BR (1999) A comparison of techniques for sampling amphibians in the forests of south-east Queensland, Australia. Herpetologica 55:271–283
Pereira HM, Ferrier S, Walters M et al (2013) Essential biodiversity variables. Science 339:277. https://doi.org/10.1126/science.1229931
Pierce BA, Gutzwiller KJ (2004) Sampling of frogs: detection efficiency in relation to survey duration. J Herpetol 38:495–500. https://doi.org/10.1670/91-04A
Pieretti N, Duarte MHL, Sousa-Lima R, Rodrigues M, Young RJ, Farina A (2015) Determining temporal sampling schemes for passive acoustic studies in different tropical ecosystems. Trop Conserv Sci 8:215–234. https://doi.org/10.1177/194008291500800117
Prado GM, Pombal JP Jr (2005) Distribuição espacial e temporal dos anuros em um brejo na Reserva Biológica de Duas Bocas, sudeste do Brasil. Arq Do Mus Nac 63:685–705
Proença V, Martin LJ, Pereira HM, Fernandez M, McRae L, Belnap J, Böhm M, Brummitt N, García-Moreno J, Gregory RD, Honrado JP, Jürgens N, Opige M, Schmeller DS, Tiago P, van Swaay CAM (2017) Global biodiversity monitoring: from data sources to Essential Biodiversity Variables. Biol Conserv 213:256–263. https://doi.org/10.1016/j.biocon.2016.07.014
R Core Team (2020) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org
Ramalho WP, Prado VHM, Signorelli L, With KA (2021) Multiple environmental filters and competition affect the spatial co-occurrence of pond-breeding anurans at both local and landscape scales in the Brazilian Cerrado. Landscape 36(6):1663–1683. https://doi.org/10.1007/s10980-021-01236-4
Ribeiro MC, Metzger JP, Martensen AC, Ponzoni FJ, Hirota MM (2009) The Brazilian Atlantic Forest: how much is left, and how is the remaining forest distributed? Implications for conservation. Biol Conserv 142:1141–1153. https://doi.org/10.1016/j.biocon.2009.02.021
Ribeiro JW, Sugai LSM, Campos-Cerqueira M (2017) Passive acoustic monitoring as a complementary strategy to assess biodiversity in the Brazilian Amazonia. Biodivers Conserv 26:2999–3002. https://doi.org/10.1007/s10531-017-1390-0
Rocha CFD, Siqueira CC, Ariani CV, Vrcibradic D, Guedes DM, Kiefer MC, Almeida-Gomes M, Goyannes-Araújo P, Borges-Júnior VNT, Van Sluys M (2015) Differential success in sampling of Atlantic Forest amphibians among different periods of the day. Braz J Biol 75:261–267. https://doi.org/10.1590/1519-6984.19412
Rödel MO, Ernst R (2004) Measuring and monitoring amphibian diversity in tropical forests I: an evaluation of methods with recommendations for standardization. Ecotropica 101:24
Ruffell J, Clout MN, Didham RK (2017) The matrix matters, but how should we manage it? Estimating the amount of high-quality matrix required to maintain biodiversity in fragmented landscapes. Ecography (cop) 40:171–178. https://doi.org/10.1111/ecog.02097
Sabbag AF, Zina J (2011) Anurofauna de uma mata ciliar no município de São Carlos, estado de São Paulo, Brasil. Biota Neotrop 11:1–10. https://doi.org/10.1590/S1676-06032011000300015
Segalla MV, Berneck B, Canedo C, Caramaschi U, Alberto Gonçalves Cruz C, Garcia PCA, Grant T, Haddad CFB, Lourenço ACC, Mângia S, Mott T, Nascimento LB, Toledo LF, Wernec FP, Langone JA (2021) List of Brazilian Amphibians. Herpetol Bras. https://doi.org/10.5281/zenodo.4716176
Sinsch U, Lümkemann K, Rosar K, Schwarz C, Dehling M (2012) Acoustic niche partitioning in an anuran community inhabiting na Afromontane wetland (Butare, Rwanda). Afr Zool 47:60–73. https://doi.org/10.1080/15627020.2012.11407524
Sgarbi LF, Bini LM, Heino J, Jyrkänkallio-Mikkola J, Landeiro VL, Santos EP, Schneck F, Siqueira T, Soininen J, Tolonen KT, Melo AS (2020) Sampling effort and information quality provided by rare and common species in estimating assemblage structure. Ecol Indic 110:105937. https://doi.org/10.1016/j.ecolind.2019.105937
Shearin AF, Calhoun AJK, Loftin CS (2012) Evaluation of listener-based anuran surveys with automated audio recording devices. Wetlands 32:737. https://doi.org/10.1007/s13157-012-0307-7
Sodhi NS, Bickford D, Diesmos AC, Lee TM, Koh LP, Brook BW, Sekercioglu CH, Bradshaw CJA (2008) Measuring the meltdown: drivers of global amphibian extinction and decline. PLoS ONE. https://doi.org/10.1371/journal.pone.0001636
Storfer A (2018) Amphibian declines: future directions. Divers Distrib 9:151–163. https://doi.org/10.1046/j.1472-4642.2003.00014.x
Stuart SN et al (2004) Status and trends of amphibian declines and extinctions worldwide. Science 306(5702):1783–1786. https://doi.org/10.1126/science.1103538
Sugai LSM, Llusia D (2019) Bioacoustic time capsules: using acoustic monitoring to document biodiversity. Ecol Indic 99:149–152. https://doi.org/10.1016/j.ecolind.2018.12.021
Sugai LSM, Silva TSF, Ribeiro JW Jr, Llusia D (2019) Terrestrial passive acoustic monitoring: review and perspectives. Bioscience 69:15. https://doi.org/10.1093/biosci/biy147
Sugai LSM, Desjonquères C, Silva TSF, Llusia D (2020) A roadmap for survey designs in terrestrial acoustic monitoring. Remote Sens Ecol Conserv 6:220–235. https://doi.org/10.1002/rse2.131
Sugai LSM, Silva TSF, Llusia D, Siqueira T (2021) Drivers of assemblage-wide calling activity in tropical anurans and the role of temporal resolution. J Anim Ecol 90:673–684. https://doi.org/10.1111/1365-2656.13399
Tabarelli M, Aguiar AV, Ribeiro MC, Metzger JP, Peres CA (2010) Prospects for biodiversity conservation in the Atlantic Forest: lessons from aging human-modified landscapes. Biol Conserv 143:2328–2340. https://doi.org/10.1016/j.biocon.2010.02.005
Thomisch K, Boebel O, Zitterbart DP, Samaran F, Van Parijs S, Van Opzeeland I (2015) Effects of subsampling of passive acoustic recordings on acoustic metrics. J Acoust Soc Am 138:267–278. https://doi.org/10.1121/1.4922703
Thompson GG, Withers PC (2003) Effect of species richness and relative abundance on the shape of the species accumulation curve. Austral Ecol 28:355–360. https://doi.org/10.1046/j.1442-9993.2003.01294.x
Ulloa JS, Aubin T, Llusia D, Courtois ÉA, Fouquet A, Gaucher P, Pavoine S, Sueur J (2019) Explosive breeding in tropical anurans: environmental triggers, community composition and acoustic structure. BMC Ecol 19:1–17. https://doi.org/10.1186/s12898-019-0243-y
Vasconcelos TS, Rossa-Feres DC (2005) Diversidade, distribuição espacial e temporal de anfíbios anuros (Amphibia, Anura) na região noroeste do Estado de São Paulo Brasil. Biota Neotrop 5(2):15. https://doi.org/10.1590/S1676-06032005000300010
Vancine MH, Duarte KS, Souza YS, Giovanelli JGR, Martins-Sobrinho PM, Lopez A, Bovo RP, Maffei F, Lion MB, Ribeiro Júnior JW, Brassaloti R, Costa COR, Sawakuchi HO, Forti LR, Cacciali P, Bertoluci J, Haddad CFB, Ribeiro MC (2018) Atlantic Amphibians: a data set of amphibian communities from the Atlantic Forests of South America. Ecology 99(7):1692. https://doi.org/10.1002/ecy.2392/suppinfo%3c/div%3e
Van Buskirk J (2012) Permeability of the landscape matrix between amphibian breeding sites. Ecol Evol 2:3160–3167. https://doi.org/10.1002/ece3.424
Wagner N, Rödder D, Brühl CA, Veith M, Lenhardt PP, Lötters S (2014) Evaluating the risk of pesticide exposure for amphibian species listed in Annex II of the European Union Habitats Directive. Biol Cons 176:64–70. https://doi.org/10.1016/j.biocon.2014.05.014
Watanabe S, Nakanishi N, Izawa M (2005) Seasonal abundance in the floor-dwelling frog fauna on iriomote island of the Ryukyu archipelago, Japan. J Trop Ecol 21:85–91. https://doi.org/10.1017/S0266467404002068
Weir LA, Mossman MJ (2005) North American Amphibian Monitoring Program (NAAMP). In: Lannoo M (ed) Amphibian declines: the conservation status of United States species. University of California Press, Berkeley, pp 307–313
Willacy RJ, Mahony M, Newell DA (2015) If a frog calls in the forest: Bioacoustic monitoring reveals the breeding phenology of the endangered Richmond Range Mountain frog (Philoria richmondensis). Austral Ecol 40:625–633. https://doi.org/10.1111/aec.12228
Wimmer J, Towsey M, Roe P, Williamson I (2013) Sampling environmental acoustic recordings to determine bird species richness. Ecol Appl 23:1419–1428. https://doi.org/10.1890/12-2088.1
Wrege PH, Rowland ED, Keen S, Shiu Y (2017) Acoustic monitoring for conservation in tropical forests: examples from forest elephants. Methods Ecol Evol 8:1292–1301. https://doi.org/10.1111/2041-210X.12730
Zina J, Ennser J, Pinheiro SCP, Haddad CFB, Toledo LF (2007) Taxocenose de anuros de uma mata semidecídua do interior do Estado de São Paulo e comparações com outras taxocenoses do Estado, sudeste do Brasil. Biota Neotrop 7(2):45. https://doi.org/10.1590/S1676-06032007000200005
Zina J, Prado CPA, Brasileiro CA, Haddad CFB (2012) Anurans of the sandy coastal plains of the Lagamar Paulista, State of São Paulo Brazil. Biota Neotrop 12(1):4. https://doi.org/10.1590/S1676-06032012000100020
Acknowledgements
We thank all farmers and landowners that generously supported the fieldwork. We also thank R. Souza, C. Loiola, and B. Vitorino for their assistance during the surveys. Permission to conduct biodiversity surveys was granted by the Brazilian Ministry of Environment (permit #51502-2). PRA thanks C.O. Gussoni for fruitful discussions on conservation. PRA was supported by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brazil (CAPES)—Finance Code 001. LSMS acknowledges grant PEJ2018-004603-A from the Spanish Ministerio de Economia, Industria y Competitividad.
Funding
PRA was supported by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brazil (CAPES) – Finance Code 001. LSMS was supported by the Spanish Ministerio de Economia, Industria y Competitividad, grant PEJ2018-004603-A.
Author information
Authors and Affiliations
Contributions
PRA, MCR, and LMTC conceived the ideas and the study design. PRA and LSMS reviewed the original ideas and hypotheses. PRA acquired field data and analyzed the acoustic data. FM curated the sound data. PRA and LSMS analyzed the data and wrote the results. PRA led the original draft and LSMS reviewed all drafts. All authors consented to the final draft.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no conflict of interest to declare.
Ethical Approval
No animals were collected or sacrificed in this study.
Consent to participate
All authors agree have reviewed and agree with the submission of this version of the manuscript.
Consent to publish
All authors accept the responsibility for releasing the material included in this manuscript.
Clinical trials registration
It does not apply to this manuscript.
Plant reproducibility
It does not apply to this manuscript.
Additional information
Communicated by Dirk Sven Schmeller.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Anunciação, P.R., Sugai, L.S.M., Martello, F. et al. Estimating the diversity of tropical anurans in fragmented landscapes with acoustic monitoring: lessons from a sampling sufficiency perspective. Biodivers Conserv 31, 3055–3074 (2022). https://doi.org/10.1007/s10531-022-02475-w
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10531-022-02475-w